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Ecological and Evolutionary Physiology of Sexual Dimorphism in Body Size in Eastern Fence Lizards
(Sceloporus undulatus)
Henry John-Alder
Department of Ecology, Evolution, and Natural Resources
School of Environmental and Biological Sciences
Morphology, Performance, and Fitness
-S. Arnold, Am. Zool. , 1983
Ultimate goal of integrative biology is to reveal the adaptive significance of phenotypic traits through their functional linkages
to fitness.
Morphology, Performance, and Fitness
-S. Arnold, Am. Zool. , 1983
“PERFORMANCE” is what animals do in nature. It is about all that
they do to work and succeed.
Statistical Relationships
“P” = phenotypic covariance
Endocrine Integration
H = hormonal pleiotropy
H14
H4K
H
H
H
H
H
H
H H
Hormones are biological agents of phenotypic covariance.
Hormones can regulate performance.
“… endocrine system interprets environmental variation to produce a range of phenotypes from the same genotype.”
Dufty, Clobert, and Møller, 2002
Sceloporus undulatus
Home Range Analysis:
Spacing Patterns and Reproductive Success
Sceloporus undulatus Eastern Fence Lizard
Unique Paint Mark for
Identification
Male Sceloporus undulatus
Home ranges are large and overlapping.
Home range area of males is 10X greater than females.
-1 0 1 2 3 40
1
2
3
4
5A.
Log Male Density (n/hectare)
Log
HR (m
2 )
Home ranges of males are large and overlapping.
Home range area depends on population density.
Home range area is an order of magnitude
greater in NJ than in other populations.
-1 0 1 2 3 40
1
2
3
4
5A.
Log Male Density (n/hectare)
Log
HR (m
2 )
Male home range
Female home ranges
Male movements
Spatial distribution of females drives movement and home range behavior of males.
Male Endurance
Apr May Jun Jul Aug Sep0
10
20
30
19941995
a
a a a a
β
α
α α α
Month
Tim
e on
Tre
adm
ill (m
in)
Running Endurance
Apr May Jun Jul Aug Sep0
10
20
30
FemaleMale
p=0.009
p<0.001
Month
Tim
e on
Tre
adm
ill (m
in) … and is greater in males
than in females during the breeding season.
Exercise endurance in males is greatest during the
breeding season …
Environmental Variation:
A “Natural Experiment”
Mar Apr May Jun Jul Aug Sep Oct0
15
30
45
60
TBMale
a
b
b,c
cb,c b,c
b,cb,c
γ γ γ γ
α
β ,γβ
γ
Month
Plas
ma
[T] o
r [B
](n
g/m
l)Male Endurance
Apr May Jun Jul Aug Sep0
10
20
30
19941995
a
a a a a
β
α
α α α
Month
Tim
e on
Tre
adm
ill (m
in)
Testosterone and corticosterone vary roughly in parallel with endurance.
Environmental Variation:
A “Natural Experiment”
Sceloporus undulatus
Exogenous testosterone ↑ endurance.
(But corticosterone has no effect.)
Experimental Manipulation
Surgical Castration
+
Testosterone Replacement
TESTOSTERONE promotes home range acquisition.
C A C O T E0
400
800
1200
1600
a
b
cHo
me R
ange
Are
a (m
2 )
1.74 1.76 1.78 1.80 1.82 1.842.5
3.0
3.5
4.0
4.5
Log Snout-Vent Length (mm)
Log
Hom
e Ra
nge
(m2 ) R2 = 0.25
p=0.016
HR area increases with body size …
1.74 1.76 1.78 1.80 1.82 1.842.5
3.0
3.5
4.0
4.5
Log Snout-Vent Length (mm)
Log
Hom
e Ra
nge
(m2 ) R2 = 0.25
p=0.016
-0.02
-0.01
0.00
0.01
0.02
2-Yr. Old
≥3-Yr. Old
Age Classp=0.003
Res
idua
l Hom
e R
ange
Are
a
… and with age. HR area increases with body size …
-0.75 -0.50 -0.25 0.00 0.25 0.50 0.75-0.50
-0.25
0.00
0.25
0.50P=0.017
Residual Home Range Area
Res
idua
l No.
of F
emal
es
Males increase their HR area by searching for females.
-0.75 -0.50 -0.25 0.00 0.25 0.50 0.75-0.50
-0.25
0.00
0.25
0.50P=0.017
Residual Home Range Area
Res
idua
l No.
of F
emal
es
Males compete for females, not for HR area per se.
Larger males sire more and larger clutches.
CORTICOSTERONE “Successful” home range behavior is strenuous
and may require high endurance.
Plasma [CORT] is correlated with
endurance:
r = 0.414, p = 0.0002, n = 76
Attainment of high fitness can be stressful.
Size Distributions of All Adults
55 60 65 70 75 800
5
10
15FemalesMales
Snout-Vent Length (mm)
p << 0.0001N
umbe
r of
Liz
ards
Index of SSD = 0.124
Sexual dimorphism in body size (SSD): an expression of body size in males relative to body size in females.
Photograph: Lukáš Kratochvíl
RMCox
Sexual Size Dimorphism (SSD) ♀ > ♂ ♂ > ♀
… while males are larger than females in many others?
Why are females larger than males in some species …
Cox, Stenquist, & Calsbeek, 2009
SSD in lizards and snakes
Aga
mid
aeC
rota
phyt
idae
Igua
nida
eP
hryn
osom
atid
aeP
olyc
hrot
idae
Tro
pidu
ridae
Var
anid
aeA
ngui
dae
Gym
noph
thal
mid
aeT
eiid
aeLa
cert
idae
Sci
ncid
aeG
ekko
nida
eP
ygop
odid
ae
-0.6
00.
60.
40.
2-0
.4-0
.2
Mal
e-b
iase
d S
SD
Fem
ale-
bias
ed S
SD
M FM FM M M M M
Nat
ricin
aeX
enod
ontin
aeC
olub
rinae
Ela
pida
eV
iper
idae
Acr
ocho
rdid
aeB
oida
eS
cole
coph
idia
-1.2
01.
20.
80.
4-0
.8-0
.4
F F F F FM
LIZARDS SNAKES
Aeluroscalabotes felinus
Paroedura picta
Crotalus atrox
Cox, Butler, & John-Alder, 2007; John-Alder, Cox, & Taylor, 2007; Cox, Stenquist, and Calsbeek, 2009; Kratochvil, Kubicka, Golinski, & John-Alder, unpubl.
S. undulatus
S. virgatus
Anolis sagrei S. jarrovii
S. magister
No Sexual Difference in Neonatal Body Size
22 25 28 31 34 37
1
3
5
7 Females Male
p=0.366
Snout-Vent Length (mm)
Num
ber o
f Liz
ards
Laboratory Hatchlings:
♀: 24.44 ± 0.08 mm
♂: 24.23 ± 0.08 mm
n = 339, p=0.063
Size Distributions of 2-Yr. Olds
55 60 65 70 75 800
5
10FemalesMales
Snout-Vent Length (mm)
p << 0.0001N
umbe
r of
Liz
ards
Index of SSD = 0.102
0.00
0.03
0.06
0.09
0.12
Index of SSD
40
60Snout-Vent (mm)
*
**
8 9 10 11 12 130.1
0.2
0.3
Growth Ratemm/day
Age (Months)
Females are larger than males by 11 months of age.
Growth rates diverge sharply between 10 and 11 months of age.
Development of SSD
0
0.02
0.04
0.06
0.08
0.1
0.12
Augus
tOct
Dec Feb
April
June
Augus
tOct
Dec Feb
April
Sexual divergence in growth is correlated with:
• ↑ Male coloration • ↑ Male aggression • ↑ Male activity
♂ ♀
Sceloporus undulatus
Correlated effects of testosterone ??
Skelly & John-Alder, Unpubl.
Experimental Enclosure
Rutgers University Pinelands Research Center, New Lisbon, NJ
Sceloporus undulatus
0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 150
10
20
30
40
50
MaleFemale
Oct May Jul Oct
11
3
11
5
A
10 114
3
Age (months)
Pla
sma
T (n
g m
l-1)
45 d 418 d0
10
20
30
40
50 (7,2) Testosterone(7,5) Castrated(6,4) Control(11) Female
F2,17 = 40.25; P < 0.001
a b b
F2,8 = 37.58; P < 0.001
a b b
F1,15 = 0.21P = 0.326
B
(age 12 mo) (age 24 mo)
Measurement Date (d post-release)
Pla
sma
T (n
g m
L-1
)
Testosterone is implicated in the development of SSD.
8 9 10 11 12 130.1
0.2
0.3
Growth Ratemm/day
Age (Months)
Cox, Skelly, & John-Alder, 2005
Castrated Female Castrated + T Intact
One Year: ~1 ng / h
300 µg
~175 µg
Scanned images of live lizards
Cox, Skelly, Leo, & John-Alder, 2005
0 10 20 30 40 50 6040
42
44
46
48
50
52
54
56
Testosterone
ControlCastrated
A (2001)
Elapsed Time (d post-release)
SV
L (m
m)
0 10 20 30 40 50 6042
44
46
48
50
52
54
56
58
Testosterone
ControlCastrated
Female
B (2002)
Elapsed Time (d post-release)
SV
L (m
m)
Testosterone Castrated Control Female0.0
0.1
0.2
0.3
a b bF3,40 = 13.71; P < 0.001
C F1,16 = 3.24; P = 0.040
8 8 9 6 6 12
Treatment/Sex Group
Gro
wth
Rat
e (m
m d
-1)
Testosterone inhibits growth in Sceloporus undulatus.
Cox, Skelly, & John-Alder, 2005
38 40 42 44 46 48 50 52 5456
58
60
62
64
66
68
CastratedControl
Testosterone
F = 41.11P < 0.001
Initial 2002 SVL (mm)
Fina
l 200
3 S
VL
(mm
)
Castration Growth; Testosterone Growth
Cox, Skelly, & John-Alder, 2005
Sceloporus undulatus
Growth Growth
Growth
Acquisition / Allocation?
↓ Food Consumption
∆ Energy Distribution
♂ ♀ ♀
♂ ♂
Smaller Pie Smaller Piece
T and Energy Acquisition
F+U estimates C in the lab.
0 1 2 3 40.00
0.05
0.10
0.15 FemaleMale ControlMale + T
Food Intake (crickets/d)
Feca
l Dry
Mas
s (g
/d)
Lab: r2 = 0.65 P < 0.001
12 10 6
T does not reduce Consumed Energy in the field or lab.
T and Energy Acquisition
F+U estimates C in the lab.
T does not affect F+U in the field.
0 1 2 3 40.00
0.05
0.10
0.15 FemaleMale ControlMale + T
Food Intake (crickets/d)
Feca
l Dry
Mas
s (g
/d)
Lab: r2 = 0.65 P < 0.001
Female Control Male Male+T0.00
0.01
0.02
0.03
0.04
Feca
l Dry
Mas
s (g
/d)
Field: F = 0.41 P = 0.67
12 10 6
T does not reduce Consumed Energy in the field or lab.
Energetic Cost of 1.5 h Activity (% Cost of Growth)
0 25 50 75 100 125 150 175 200
S. undulatus
S. graciosus
S. occidentalis
S. variabilis
S. virgatus
S. occidentalis
S. variabilis
S. virgatus
S. virgatus
S. virgatus
Mean
a
a
Summer Juveniles
Summer Adults
Spring Adults
Spring Juveniles
Fall Adults
Bastonal Adults
Monte Pio Adults
Spring Males
Spring Females
Summer Males
Summer Females
S. occidentalis
ThermalIncrement in RMR
Cost ofFree Existence
0 20 40 60 80 100 120 140
Energetic Cost of Growth
Energetic Cost of 1.5 h Activity (J)
Sce
lopo
rus
Spe
cies
Testosterone stimulates activity and a 1.5 h extension in active day length.
This bar is our literature-based estimate of the
cost of 1.5 h of activity.
Cox, Skelly, & John-Alder, 2005
Energetic Cost of 1.5 h Activity (% Cost of Growth)
0 25 50 75 100 125 150 175 200
S. undulatus
S. graciosus
S. occidentalis
S. variabilis
S. virgatus
S. occidentalis
S. variabilis
S. virgatus
S. virgatus
S. virgatus
Mean
a
a
Summer Juveniles
Summer Adults
Spring Adults
Spring Juveniles
Fall Adults
Bastonal Adults
Monte Pio Adults
Spring Males
Spring Females
Summer Males
Summer Females
S. occidentalis
ThermalIncrement in RMR
Cost ofFree Existence
0 20 40 60 80 100 120 140
Energetic Cost of Growth
Energetic Cost of 1.5 h Activity (J)
Sce
lopo
rus
Spe
cies
Our estimate of energy expenditure is validated by these doubly-labeled water measurements of field metabolism in lizards.
Cox, Skelly, & John-Alder, 2005
Female-larger S. undulatus
Testosterone increases:
Maintenance Growth Activity, Movement, etc.
Maintenance Growth Activity, Movement, Home Range
Maintenance Growth Activity, Movement, etc.
Available Energy
TEST CON
CAST
Energy Allocation Trade-Off
CAST CON TEST0
2
4
6
8
10
12
a ab
Daily
Act
ivity
Per
iod
(h d
-1)
CAST CON TEST0
20
40
60
80
a a
b
Daily
Mov
emen
t (m
d-1
)
CAST CON TEST0
400
800
1200
1600
a
b
c
Hom
e Ra
nge
Area
(m2 )
Activity Period Movement Home Range Area
Cox, Skelly, & John-Alder (2005) Physiol. Biochem. Zool.
Female-larger Sceloporus virgatus
37 39 41 43 45 47 49 51 53
0.00
0.05
0.10
0.15
0.20
0.25
0.30
TESTCAST
Initial SVL (mm)
Gro
wth
Rat
e (m
m/d
)
p
S. virgatus S. jarrovii
b
a
α
β
Species
Male-larger Sceloporus jarrovii
48 50 52 54 56 58 60 62
TEST
CAST
0.00
0.05
0.10
0.15
0.20
0.25
0.30
Initial SVL (mm)
Grow
th Rate (m
m/d)
S. virgatus
SSD: ♀ > ♂
S. jarrovii
SSD: ♂ > ♀
Bipotential Growth Regulation Hypothesis
SSD Effect of T
none
Species Study
Psammodromus algirus
Thamnophis sirtalis
Anolis sagrei
Urosaurus ornatus
Sceloporus undulatus
Sceloporus virgatus
Sceloporus jarrovii
Salvador & Veiga 2000
Crews et al. 1985 Lerner & Mason 2001
Cox et al. 2009
Hews et al. 1994 Hews & Moore 1995
Klukowski et al. 1996 Cox et al. 2005
Abell 1998 Cox & John-Alder 2005
Cox & John-Alder 2005
Cox, Stenquist, & Calsbeek, 2009
Photograph: Lukáš Kratochvíl
Special thanks to: Bob Cox (UVa), Christine Duncan (Fresno State), Greg
Haenel (Elon Univ), Linda Smith (Richard Stockton College)
Major funding from: National Science Foundation Society for Integrative and Comparative Biology Rutgers University